Hyper-conserved sperm proteins can still evolve rapidly

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The fastest-evolving genes in eukaryotes commonly encode reproductive proteins—and the rate at which genes for male reproductive proteins change, in particular, often vastly outstrips the rate of change across the genome as a whole.

A recent paper in G3: Genes|Genomes|Genetics describes an unusual exception: the amino acid sequences of the most abundant sperm proteins in many nematodes are almost completely static. Authors Katja Kasimatis and Patrick Phillips found that the amino acid sequences of these major sperm proteins (MSPs) are some of the most conserved of any known protein in any organism; their glacial rate of change is on par with that of essential proteins like the histones that act as spools for genomic DNA.

Despite defying the expectation that sperm proteins should evolve rapidly due to sperm competition and coevolution with egg proteins, the sluggish rate of MSP sequence change can be explained. Like many sperm proteins, MSPs are pleiotropic—that is, they have more than one job, and these functions are sometimes seemingly unrelated. In addition to being essential for sperm movement, MSPs act as signaling molecules in eggs, meaning that any sequence changes that improve sperm motility could also affect egg function, and not necessarily in a positive way.

MSPs may be frozen by pleiotropy at the sequence level, but it wouldn’t be accurate to say they’re not evolving. Taking a zoomed-out view of the whole genomes of several nematode species, Kasimatis and Phillips saw that genes for MSPs aren’t fixed at all: over evolutionary time, they have changed dramatically in copy number and have even jumped from chromosome to chromosome. Variations like these can have functional relevance, since copy number changes can alter the amount of protein produced from a gene, and changing the location of a gene within the genome can alter its regulation.

This peculiar example shows how reproductive proteins are driven to evolve rapidly, even when their sequences are constrained to an extreme degree—and demonstrates how a broader view of entire genomes and gene family dynamics is sometimes critical for understanding a gene’s evolutionary history.